OBJECTIVE:
To analyze the underreporting of the tuberculosis (TB) and AIDS comorbidity.METHODS: Surveillance study using records from the Notifiable Diseases
Information System - Tuberculosis and AIDS in Brazil from 2000 to 2005. Records
of TB without information on the presence of Aids were considered to be underreporting
of the comorbidity when paired off with AIDS records in which the year of diagnosis
of AIDS was the same or previous to the year of reporting of TB, as well as
records from the same patient whose previous records had this information. An
indicator was created: recognized TB-AIDS comorbidity, based on the TB records
that had information on the presence of AIDS.RESULTS: The underreporting of TB-AIDS was 17.7%. This percentage varied
between states. The incorporation of the underreported records into the previously
recognized ones increased the proportion of TB-AIDS in Brazil from 6.9% to 8.4%.
The highest proportions of underreporting were noted in Acre (Northern), Alagoas,
Maranhão and Piauí (Northeastern) (more than 35% each) and the
lowest in São Paulo (Southeastern) and Goiás (Central-western)
(around 10% each).CONCLUSIONS: The underreporting of the TB-AIDS comorbidity found in Brazil
will probably trigger modifications in the surveillance system in order to provide
information for the national programs.

Underreporting
of a health condition whose reporting is compulsory occurs when a case is not
reported to the information system, or when it occurs outside the established
period.9 Wrong estimates of the magnitude of diseases may derive
from this, which negatively affects the planning of prevention and control strategies
and may lead to under allocation of actions and resources.11

The epidemiological
surveillance system of communicable diseases in Brazil is routinely passive.
The lack of knowledge of health professionals about which diseases to report
and about the reporting flow, as well as changes in the case definition and
the belief that another professional has reported the case, may contribute to
the underreporting of cases.3,ª
In addition, patients or their relatives sometimes request secrecy in relation
to the diagnosis of diseases like tuberculosis (TB) and AIDS, even though they
know it is a necessary information for official purposes.9

The coinfection
by the TB bacillus and the human immunodeficiency virus (HIV), and their mutual
interference in the evolution of TB and AIDS, have demanded the strengthening
of the surveillance network in Brazil. The Programa Nacional de Controle
da TB (PNCT - National Program for TB Control) and the program directed
at sexually transmissible diseases (STD/AIDS) started to establish joint epidemiological
surveillance strategies in 2004 and made obligatory the offer of the HIV test
for new TB cases, with the need of the patient's consent to testing. However,
the magnitude of the association between these two diseases may not be apparent
if comorbidity cases are not reported.1

The aim of the
study was to analyze the underreporting of the TB-AIDS comorbidity in Brazil.

METHODS

Surveillance study
with data from Sistema de Informação de Agravos de Notificação
de Tuberculose (SINAN-TB - National Information System for Tuberculosis
Notification) from 2000 to 2005 and from the AIDS national database from 1980
to 2005. This database results from the consolidation of information systems
such as: Sistema de Informação de Agravos de Notificação
de Aids (SINAN-AIDS - National Information System for AIDS Notification),
Sistema de Controle de Exames Laboratoriais (SISCEL - Laboratory Tests
Control System), Sistema de Controle Logístico de Medicamentos
(SICLOM - System for Logistic Control of Medicines), Sistema de Informação
de Mortalidade (SIM - Mortality Information System).7

The SINAN-TB database
was extracted in February 2007 and the AIDS national database in April 2007.
Both underwent data quality analysis for the recognition, classification and
removal of duplicate records (presence of more than one record of the same patient)
by means of probabilistic linkage, as described in the literature.2,10

The depuration
process applied to SINAN-TB respected the structural logic of SINAN, according
to which records of patients in the first treatment episode or in subsequent
treatment episodes (retreatments due to return after default or relapse after
cure) should be maintained. Records of the same patient in one treatment episode,
but coming from different healthcare units were linked (transfers). Records
of the same patient in different treatment episodes were maintained in the database,
chronologically ordered by date of diagnosis, report and treatment onset. For
the linkage with SINAN-AIDS, the first record of each patient was used.

In the structural
logic of the AIDS national database, each patient should have only one record.
This database had 419,795 records, each referring to one patient. Of this total,
99,276 (23.7%) had died before 2000 (current situation/date of death) and were
not used for the linkage.

The linkage between
databases was performed in two consecutive cycles, the second to enhance linkage
sensitivity. The first cycle had three stages: pre-processing of the database,
probabilistic linkage and identification of true matching pairs. In pre-processing,
the databases underwent reformatting of the variables: date of report; date
of diagnosis; date of birth; and corrections in the variables: patient's name;
patient's mother's name. Besides, the most common non-discriminatory addresses
were removed, like those of the penitentiary system, and any mentions referring
to the patient not having a home or that it was unknown (homeless, street dweller,
etc.). In the probabilistic linkage, the following variables were used: patient's
name, mother's name, and date of birth. The sex variable was used to divide
the databases into smaller blocks and increase linkage speed. The probabilities
used in the linkage were extracted by indirect method. The identification of
linked records was performed by the program Link Plus,b
which calculates the probability of agreement and disagreement of the variables
selected for linkage. The higher the score, the higher the probability that
the linked pair refer to the same individual. The value three was empirically
defined as the cutoff point, above which the program should list the linked
pairs. True matching pairs were the ones in which both records belonged to the
same individual, confirmed by manual depuration. To achieve this, information
on age was also considered, as well as federative unit, municipality of residence,
street and number. When in doubt, we decided on the conservative alternative
of not considering the linked records as true matching pairs. Manual revision
was carried out on pairs with scores from three to 13.5. Those with scores from
13.5 to 23.5 (the highest value found) were considered true matching pairs without
manual revision.

There were many
records in the AIDS national database with TB diagnosis not linked with the
SINAN-TB. Thus, a new linkage cycle was performed of these records with those
of SINAN-TB with HIV-positive and/or AIDS associated health condition. The program's
configuration parameters were altered and patient's name and date of birth were
chosen as linkage variables. Sex remained as the blocking variable and the cutoff
point was altered to 0.1. After a new manual depuration, the true matching pairs
were tagged in the original databases of SINAN-TB and AIDS.

The comorbidity
records identified in SINAN-TB belonged to four types:

type 1 - first
or only record of each patient linked to a record of the AIDS national database;

type 2 - patients
with multiple records, with the first linked to a record of the AIDS national
database. In case of linkage between one record of SINAN-TB and the AIDS database,
all records of the same patient were considered linked. If the year of TB
report was previous to the year of AIDS diagnosis, the record would not be
considered TB-AIDS because, in 2000, pulmonary TB (the most prevalent form
of the disease) was not considered an AIDS defining condition in the CDC Modified
criterion;12 thus, these records might characterize a coinfection
condition and not a comorbidity;

type 3 - health
conditions associated with AIDS not linked to the AIDS national database,
i.e., which were not type 1 or 2. This variable should be filled with one
of the mutually exclusive values: AIDS, alcoholism, mental disease, diabetes
and others;

type 4 - without
information on AIDS associated health condition, not found by means of linkage
with the AIDS national database, but with information on AIDS associated health
condition in one of the previous records of the same patient.

The identified
TB-AIDS records (sum of type 1 to 4 records) were classified into two conditions:
a) recognized comorbidity, in which the information that the patient had AIDS
was filled in the variable associated health conditions, and b) underreporting
of the comorbidity, in which the information that the patient had AIDS was not
filled for this variable.

Possible associations
were analyzed between recognized comorbidity or underreporting and sex, age
group, type of admission (new case, relapse, return after default and transfer),
clinical form (pulmonary, extrapulmonary, pulmonary + extrapulmonary), HIV status
(positive, negative, ongoing, not performed or without information), sputum
bacilloscopy (positive, negative, not performed) and treatment outcome (cure,
default, death, transfer or multiresistant TB). The chi-square test was employed
to evaluate statistically significant differences between levels of these variables.
The completeness of the variables HIV and associated health conditions was also
analyzed.

The results obtained
in the linkage were made available to health professionals involved in epidemiological
surveillance actions. Individuals' identification data used in the linkage were
not disclosed, ensuring the secrecy and confidentiality of this information.

The statistical
program Stata 9.0 was utilized in the pre-processing of the database, in the
manual depuration of the pairs, in the tagging of the true matching pairs in
the original databases and in the analysis.

A total of 5,009
type 2 comorbidity records were found, followed by 8,460 type 3 records and
631 type 4 records. Of 43,404 comorbidity records in the sum of the four types,
35,728 (82.3%) were of comorbidity with information of AIDS associated health
condition, and 7,676 (17.7%) were underreporting recognized by linkage (16.2%)
or because they were multiple records of patients with information of AIDS associated
health condition in a previous record (1.5%) (Figure
1).

A total of 8,804
records was identified in the AIDS national database from 2000 to 2005 that
presented TB at the moment of the diagnosis, but not linked to records of SINAN-TB
and, consequently, not considered comorbidity cases.

The proportion
of underreporting was gradually reduced throughout the studied period, with
a mean of 17.7% in the entire period. The proportion of recognized comorbidity
was 6.9% and rose to 8.4% (a 21.4% increase; Table
1). The highest underreporting proportions were observed in Acre, Alagoas,
Maranhão and Piauí (more than 35% each) and the lowest in São
Paulo and Goiás (around 10% each) (Figure 2).

Records of recognized
comorbidity and underreporting had distinct characteristics for all the studied
variables. The underreporting records presented more advanced age, predominance
of new cases, of the pulmonary clinical form, of positive sputum bacilloscopy,
of negative HIV test result and of default as outcome. These differences were
more remarkable for HIV status and clinical form of TB: while the records of
recognized comorbidity presented 93.9% (and not 100%) of HIV-positive result
and 58.6% of pulmonary clinical form, the comorbidity underreporting records
presented 58.3% of HIV-positive and 70.3% of pulmonary clinical form (Table
2).

Although the proportion
of records without information on associated health conditions decreased throughout
the period, it still represented the majority of records in 2005 (74.8%). The
proportion of records without information on HIV status also decreased over
the studied period, reaching 64% in 2005 (Table
3).

DISCUSSION

This study estimated
17.7% of underreporting of the TB-AIDS comorbidity, a phenomenon that has already
been described for TB-AIDS and other diseases.3,7,9,c

Reporting reliable
number of patients with TB-AIDS is essential for the adequate planning of control
measures and to provide efficient care for the patient. In addition, a very
serious matter would be characterized if TB cases with AIDS might not have been
identified by PNCT for patients whose records lacked the comorbidity information.
The information on the presence of the comorbidity is fundamental to inform
the follow-up of the patients, since the natural history of TB is modified by
AIDS, with increase in recurrence, as well as its clinical presentation, treatment
duration and tolerance and resistance against the available drugs.6,8,d

To increase the
completeness of the health conditions associated with AIDS, it is important
to increase the completeness of the HIV status variable. The health professionals
that follow the case up and the ones who fill in the follow-up card of SINAN-TB
must pay attention to fill in the health conditions associated with AIDS in
the records of HIV-positive patients. It is necessary not only to ensure the
performance of the test for all those who consent to it, but also to ensure
that the results are entered into the information systems as soon as they are
available. The lower the proportion of patients with TB tested for HIV and HIV-positive
patients reported in SINAN-TB, the higher the uncertainty about the real prevalence
of HIV among TB patients. According to SINAN-TB data, the prevalence of HIV
would be 8.2% in 2005, below the 14% that had been estimated by the World Health
Organization (WHO) for Brazil for the same year.e

PNCT is responsible
for feedbacking the analyses of notification data to the health professionals
that follow up cases and fill in the reports so that they understand the importance
of filling in the records adequately and feel motivated to improve the quality
of the collected data. Furthermore, it is essential that these professionals
are instructed in topics of TB epidemiology that are important to the execution
of their work. For example, they should be warned that, although patients with
extrapulmonary TB have higher risk of having the TB-AIDS comorbidity,4
those with pulmonary TB may also present it, and therefore the comorbidity information
should be reported both to the extrapulmonary and to the pulmonary forms, which
was not happening properly.

The modification
of the variable "associated health conditions" was identified as one of the
necessary measures to improve the data entry process. Given the structure of
the variable, it was possible to inform the presence of only one health condition
at a time. This modification has already been incorporated into the last versions
of SINAN-TB, in which each comorbidity is now registered in a specific field,
marked with the values that indicate its presence, absence or lack of information.f

The main measure
to prevent the underreporting of the comorbidity in SINAN-TB would be to enhance
collaboration between the control programs, as recommended by the WHO.d
Information exchange between the two programs should occur routinely in all
administrative levels to ensure knowledge of the comorbidity condition and early
access to measures of prevention and treatment.

The probabilistic
linkage between the databases of SINAN-TB and the AIDS national database may
contribute to improve the quality of their data. The underreporting of TB-AIDS
per federation unit presented here can be compared to that of places that introduce
the measures proposed here to prevent this underreporting. Periodicity and the
administrative level responsible for the linkage should be defined taking into
account the burden of both diseases and the availability and local capacity
of human resources, in view of the fact that this activity demands time and
relatively skilled work. The comorbidity condition described by the linkage
at any level must be immediately transferred to the healthcare units responsible
for the follow-up and reporting of the cases.

In relation to
the limitations of the study, false records of comorbidity underreporting may
have been identified if linked records were erroneously considered as being
of the same patient. This situation is improbable given the rigorous manual
depuration that was performed. Problems in the quality of the information of
the variables selected to the linkage or limitations intrinsic to the Link Plus
program may have compromised the identification of records of comorbidity underreporting.
There is no gold standard that allows ascertaining the sensitivity of this program.
These reasons may explain at least part of the 8,804 records in the AIDS national
bank from 2000 to 2005 with TB when AIDS was diagnosed that were not linked
to SINAN-TB. Another possibility is the non-existence of records corresponding
to the AIDS national database in SINAN-TB, which would denote underreporting
not only of the comorbidity condition, but also of the reporting of the TB case.
This amount was not added to the total comorbidity records to avoid duplication
of cases, which would happen if the correspondents records of SINAN-TB also
indicated AIDS. However, if added, the comorbidity proportion of the total TB
records would rise from 6.9% to 10.1%, and the underreporting from 17.7% to
38%. The real proportion of comorbidity underreporting should be understood
within this interval.

Another possible
limitation of the study would be the non-utilization of the capture-recapture
method, which, in theory, would estimate the total of TB-AIDS cases in Brazil
beyond those contained in the studied databases. We chose not to use this method
due to the absence of a third source of TB-AIDS data. The use of more than two
data sources is essential so that these studies are considered valid. Without
this, it is impossible to ascertain and control for independence between sources,
which is one of its fundamental premises.5

The underreporting
of the TB-AIDS comorbidity in Brazil will probably trigger modifications in
the surveillance system of these health conditions that offer information to
national programs. This information is essential to enhance the quality of the
system regarding the development of activities of data collection and analysis,
besides greater incentive to and valuation of the health professionals.